ABSTRACT Plant roots shape the rhizosphere community by secreting compounds that recruit diverse bacteria. Colonization of various plant roots by the motile alphaproteobacterium Azospirillum brasilens e causes increased plant growth, root volume, and crop yield. Bacterial chemotaxis in this and other motile soil bacteria is critical for competitive colonization of the root surfaces. The role of chemotaxis in root surface colonization has previously been established by endpoint analyses of bacterial colonization levels detected a few hours to days after inoculation. More recently, microfluidic devices have been used to study plant-microbe interactions, but these devices are size limited. Here, we use a novel slide-in chamber that allows real-time monitoring of plant-microbe interactions using agriculturally relevant seedlings to characterize how bacterial chemotaxis mediates plant root surface colonization during the association of A. brasilens e with Triticum aestivum (wheat) and Medicago sativa (alfalfa) seedlings. We track A. brasilense accumulation in the rhizosphere and on the root surfaces of wheat and alfalfa. A. brasilense motile cells display distinct chemotaxis behaviors in different regions of the roots, including attractant and repellent responses that ultimately drive surface colonization patterns. We also combine these observations with real-time analyses of behaviors of wild-type and mutant strains to link chemotaxis responses to distinct chemicals identified in root exudates to specific chemoreceptors that together explain the chemotactic response of motile cells in different regions of the roots. Furthermore, the bacterial second messenger c-di-GMP modulates these chemotaxis responses. Together, these findings illustrate dynamic bacterial chemotaxis responses to rhizosphere gradients that guide root surface colonization. IMPORTANCE Plant root exudates play critical roles in shaping rhizosphere microbial communities, and the ability of motile bacteria to respond to these gradients mediates competitive colonization of root surfaces. Root exudates are complex chemical mixtures that are spatially and temporally dynamic. Identifying the exact chemical(s) that mediates the recruitment of soil bacteria to specific regions of the roots is thus challenging. Here, we connect patterns of bacterial chemotaxis responses and sensing by chemoreceptors to chemicals found in root exudate gradients and identify key chemical signals that shape root surface colonization in different plants and regions of the roots.
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The Arabidopsis LHT1 Amino Acid Transporter Contributes to Pseudomonas simiae-Mediated Plant Growth Promotion by Modulating Bacterial Metabolism in the Rhizosphere
The root microbiome structure ensures optimal plant host health and fitness, and it is, at least in part, defined by the plant genotype. It is well documented that root-secreted amino acids promote microbial chemotaxis and growth in the rhizosphere. However, whether the plant-mediated re-uptake of amino acids contributes to maintaining optimal levels of amino acids in the root exudates, and, in turn, microbial growth and metabolism, remains to be established. Here, we show that Lysine-Histidine Transporter-1 (LHT1), an amino acid inward transporter expressed in Arabidopsis thaliana roots, limits the growth of the plant-growth-promoting bacteria Pseudomonas simiae WCS417r (Ps WCS417r). The amino acid profiling of the lht1 mutant root exudates showed increased levels of glutamine, among other amino acids. Interestingly, lht1 exudates or Gln-supplemented wild-type exudates enhance Ps WCS417r growth. However, despite promoting bacterial growth and robust root colonization, lht1 exudates and Gln-supplemented wild-type exudates inhibited plant growth in a Ps WCS417r-dependent manner. The transcriptional analysis of defense and growth marker genes revealed that plant growth inhibition was not linked to the elicitation of plant defense but likely to the impact of Ps WCS417r amino acids metabolism on auxin signaling. These data suggest that an excess of amino acids in the rhizosphere impacts Ps WCS417r metabolism, which, in turn, inhibits plant growth. Together, these results show that LHT1 regulates the amino-acid-mediated interaction between plants and Ps WCS417r and suggest a complex relationship between root-exuded amino acids, root colonization by beneficial bacteria, bacterial metabolism, and plant growth promotion.
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- Award ID(s):
- 1943120
- NSF-PAR ID:
- 10417946
- Date Published:
- Journal Name:
- Plants
- Volume:
- 12
- Issue:
- 2
- ISSN:
- 2223-7747
- Page Range / eLocation ID:
- 371
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/plants12020371
